Abstract

Climate change influences population demography by altering patterns of gene flow and reproductive isolation. Direct mutation rates offer the possibility for accurate dating on the within-species level but are currently only available for a handful of vertebrate species. Here, we use the first directly estimated mutation rate in birds to study the evolutionary history of pied flycatchers (Ficedula hypoleuca). Using a combination of demographic inference and species distribution modelling, we show that all major population splits in this forest-dependent system occurred during periods of increased climate instability and rapid global temperature change. We show that the divergent Spanish subspecies originated during the Eemian–Weichselian transition 115–104 thousand years ago (kya), and not during the last glacial maximum (26.5–19 kya), as previously suggested. The magnitude and rates of climate change during the glacial–interglacial transitions that preceded population splits in pied flycatchers were similar to, or exceeded, those predicted to occur in the course of the current, human-induced climate crisis. As such, our results provide a timely reminder of the strong impact that episodes of climate instability and rapid temperature changes can have on species' evolutionary trajectories, with important implications for the natural world in the Anthropocene.

Highlights

  • Climate change can promote lineage divergence by introducing vicariant barriers that result in altered patterns of gene flow, hybridization and selection across the landscape [1]

  • Variant calling in ANGSD (-doMaf 2) yielded 79 918 sites with a minor allele frequency (MAF) significantly different from zero at a p-value < 0.000001

  • PCA identified three genetic clusters: a distinct cluster consisting of all six individuals sampled in central Spain (‘E’, brown), a distinct cluster consisting of 12 of the 15 individuals royalsocietypublishing.org/journal/rspb Proc

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Summary

Introduction

Climate change can promote lineage divergence by introducing vicariant barriers that result in altered patterns of gene flow, hybridization and selection across the landscape [1]. It is well established that Quaternary climate change has profoundly impacted on today’s biota, causing widespread extinctions in some taxa and promoting lineage diversification in others, thereby shaping global patterns of biodiversity [3,4,5]. In most cases, large confidence intervals around divergence time estimates from genetic data make it impossible to link species divergence to such narrow intervals, let alone individual climate cycles. These uncertainties prevent us from assessing the impact of different climate change metrics (velocity, duration, geographic scale, magnitude) on past, and potentially future, biota

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